Hundreds of aquatic vertebrates perform extensive migrations between specific locales or habitats. Although it is well known that many of these directed movements are guided by chemical cues, their specific identities have not yet been clearly established. Nevertheless, two distinct processes have been elucidated. In one, juveniles learn complex suites of compounds in their natal environment which they later recognize when they re-encounter them as migratory adults (e.g., salmon, sea turtles). In the other, migrating individuals instinctively recognize cues that have some inherent ecological relevance (e.g., eels, lamprey). Chemicals released by members of the same species (i.e., pheromones) frequently play a critical role in the later process, likely because habitat quality and species abundance are typically correlated. Herein, we define pheromones (which have historically been defined in many ways (Sorensen and Wyatt Corsini Encyclopedia of Psychology and Behavioral Science, Wiley (2001)) as “substances that are secreted to the outside by an individual and received by a second individual of the same species, in which they release a specific reaction, for example, a definite behaviour or developmental process” (Karlson and Luscher, Nature, 183: 55-56 (1959)).
The sea lamprey is an appropriate and fascinating species to investigate pheromonally mediated migration. One of the few survivors from early vertebrate evolution, it possesses an exceptionally large olfactory system that it employs to mediate all aspects of its life. The sea lamprey is also a destructive pest in the Finger Lakes of New York and New England (Lake Champlain, Lake Oneida, and Lake Cayauga in particular) and in the Laurentian Great Lakes. Sea lampreys invaded these systems in the early 20th century where they quickly established themselves and drove many fishes to extinction. Although the fisheries of the Great Lakes have partially recovered since the implementation of a control program based on larval poisons, new and better means to control sea lamprey are sought. Their migratory life history offers specific opportunities for control. Adult sea lamprey spawn in freshwater streams where its eyeless larvae then reside for 3-20 years before metamorphosing into a parasitic phase that migrates downstream to oceans/large lakes to find hosts. Parasitic lamprey are transported by hosts great distances before they mature and seek out spawning streams, which they then enter to find mates, spawn, and die. Studies of free-ranging adults demonstrate that stream finding is guided by olfactory cues. Further, fisheries catch data have long suggested that these cues originate from stream-resident larvae (i.e., pheromones) since adults do not return to natal streams but instead exhibit strong biases for streams containing larvae (Vrieze and Sorensen, Can. J. Fish Aquat. Sci., 58:2374-2385 (2001); Sorensen et al. J Great Lakes Res, 29 (Supplement 1): 66-84 (2003)).
More direct evidence of pheromonal attractants results from studies showing larval holding water to be remarkably attractive (a 1 g larva activates over 300 liters of water an hour) and to alter the choices of adults for stream waters (Vrieze and Sorensen, Can. J. Fish Aquat. Sci., 58:2374-2385 (2001)). Efforts to identify structural aspects of the lamprey migratory pheromone began a decade ago when it was hypothesized that a unique bile acid, petromyzonol sulfate (1) already known to be produced by larval lamprey (Haslewood et al., J. Biochem., 114, 179-184 (1969)), might be released to the water to function as a pheromone (Sorensen et al., J. Great Lakes Res., 29 (Supplement 1):66-84 (2003)). It was subsequently demonstrated that larval lamprey release significant quantities of 1, along with lesser quantities of its likely precursor, allocholic acid (ACA), and that the adult lamprey olfactory system detects these products with high specificity at 10−12 and 10−11 Molar (M) (Polkinghorne et al., Fish Physiol. Biochem., 24, 15-30 (2001); Li et al., J. Gen. Physiol., 105, 569-589 (1995)); and Li et al., J. Comp Physiol. A., 180, 429-438 (1997)). Behavioural tests using a large maze and natural waters also found a mixture of 1 and ACA to be attractive (Vrieze et al., Can. J. Fish. Aquat. Sci., 58, 2374-2385 (2001)), while electrospray ionization mass spectrometry (ESI-MS) identified 1 (but not ACA) in river water at concentrations ranging up to 10−11 M. However, these studies also found responses to 1 and/or ACA to be weaker than those to larval holding water, suggesting that the larval pheromone, like most insect pheromones, is a complex mixture.